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Predictors of Invasive Adenocarcinomas Among Pure Ground-Glass Nodules Less Than 2 Cm in Diameter

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Predictors of Invasive Adenocarcinomas Among Pure Ground-Glass Nodules Less Than 2 Cm in Diameter cancers Article Predictors of Invasive Adenocarcinomas among Pure Ground-Glass Nodules Less Than 2 cm in Diameter Wen-Chi Hsu 1, Pei-Ching Huang 1, Kuang-Tse Pan 1, Wen-Yu Chuang 2 , Ching-Yang Wu 3 , Ho-Fai Wong 1, Cheng-Ta Yang 4 and Yung-Liang Wan 1,* 1 Department of Medical Imaging and Intervention, Linkou Chang Gung Memorial Hospital, College of Medicine, Chang Gung University, Taoyuan 333, Taiwan; [email protected] (W.-C.H.); [email protected] (P.-C.H.); [email protected] (K.-T.P.); [email protected] (H.-F.W.) 2 Department of Anatomic Pathology, Linkou Chang Gung Memorial Hospital, College of Medicine, Chang Gung University, Taoyuan 333, Taiwan; [email protected] 3 Division of Thoracic and Cardiovascular Surgery, Linkou Chang Gung Memorial Hospital, College of Medicine, Chang Gung University, Taoyuan 333, Taiwan; [email protected] 4 Department of Thoracic Medicine, Chang Gung Memorial Hospital, Taoyuan 333, Taiwan; [email protected] * Correspondence: [email protected]; Tel.: +886-3-3281200 (ext. 2575) Simple Summary: Benign lesions, atypical adenomatous hyperplasia, and malignancies such as adenocarcinoma in situ, minimally invasive adenocarcinoma, and invasive adenocarcinoma may feature pure ground-glass nodules on chest CT images, and the prognosis of patients with invasive adenocarcinoma is worse than others. The early detection and adequate management of invasive Citation: Hsu, W.-C.; Huang, P.-C.; adenocarcinoma is crucial, but the pathology diagnosis of small nodules is difficult to obtain without Pan, K.-T.; Chuang, W.-Y.; Wu, C.-Y.; surgery. Our study aimed to analyze the CT characteristics of pure ground-glass nodules <2 cm Wong, H.-F.; Yang, C.-T.; Wan, Y.-L. for the identification of invasive adenocarcinomas. A total of 181 nodules in 171 patients were Predictors of Invasive enrolled. The larger size, lobulation, and air cavity were significantly more common in invasive Adenocarcinomas among Pure adenocarcinoma. The air cavity is the significant predictor in multivariate analysis. In conclusion, the Ground-Glass Nodules Less Than 2 possibility of invasive adenocarcinoma is higher in a pure ground-glass nodules when it is associated cm in Diameter. Cancers 2021, 13, with a larger size, lobulation, and air cavity. 3945. https://doi.org/10.3390/ cancers13163945 Abstract: Benign lesions, atypical adenomatous hyperplasia (AAH), and malignancies such as ade- nocarcinoma in situ (AIS), minimally invasive adenocarcinoma (MIA), and invasive adenocarcinoma Academic Editors: Giuseppe Broggi (IA) may feature a pure ground-glass nodule (pGGN) on a thin-slide computed tomography (CT) and Lucia Salvatorelli image. According to the World Health Organization (WHO) classification for lung cancer, the prog- nosis of patients with IA is worse than those with AIS and MIA. It is relatively risky to perform a Received: 30 June 2021 Accepted: 2 August 2021 core needle biopsy of a pGGN less than 2 cm to obtain a reliable pathological diagnosis. The early Published: 5 August 2021 and adequate management of patients with IA may provide a favorable prognosis. This study aimed to disclose suggestive signs of CT to accurately predict IA among the pGGNs. A total of 181 pGGNs Publisher’s Note: MDPI stays neutral of less than 2 cm, in 171 patients who had preoperative CT-guided localization for surgical excision with regard to jurisdictional claims in of a lung nodule between December 2013 and August 2019, were enrolled. All had CT images of published maps and institutional affil- 0.625 mm slice thickness during CT-guided intervention to confirm that the nodules were purely iations. ground glass. The clinical data, CT images, and pathological reports of those 171 patients were reviewed. The CT findings of pGGNs including the location, the maximal diameter in the long axis (size-L), the maximal short axis diameter perpendicular to the size-L (size-S), and the mean value of long and short axis diameters (size-M), internal content, shape, interface, margin, lobulation, Copyright: © 2021 by the authors. spiculation, air cavity, vessel relationship, and pleural retraction were recorded and analyzed. The Licensee MDPI, Basel, Switzerland. final pathological diagnoses of the 181 pGGNs comprised 29 benign nodules, 14 AAHs, 25 AISs, This article is an open access article 55 MIAs, and 58 IAs. Statistical analysis showed that there were significant differences among distributed under the terms and the aforementioned five groups with respect to size-L, size-S, and size-M (p = 0.029, 0.043, 0.025, conditions of the Creative Commons respectively). In the univariate analysis, there were significant differences between the invasive Attribution (CC BY) license (https:// adenocarcinomas and the non-invasive adenocarcinomas with respect to the size-L, size-S, size-M, creativecommons.org/licenses/by/ lobulation, and air cavity (p = 0.009, 0.016, 0.008, 0.031, 0.004, respectively) between the invasive 4.0/). Cancers 2021, 13, 3945. https://doi.org/10.3390/cancers13163945 https://www.mdpi.com/journal/cancers Cancers 2021, 13, 3945 2 of 12 adenocarcinomas and the non-invasive adenocarcinomas. The receiver operating characteristic (ROC) curve of size for discriminating invasive adenocarcinoma also revealed similar area under curve (AUC) values among size-L (0.620), size-S (0.614), and size-M (0.623). The cut-off value of 7 mm in size-M had a sensitivity of 50.0% and a specificity of 76.4% for detecting IAs. In the multivariate analysis, the presence of air cavity was a significant predictor of IA (p = 0.042). In conclusion, the possibility of IA is higher in a pGGN when it is associated with a larger size, lobulation, and air cavity. The air cavity is the significant predictor of IA. Keywords: ground-glass nodule; CT; predictor; invasive adenocarcinoma; non-invasive adenocarci- noma; pre-invasive lesion 1. Introduction Lung cancer was the leading cause of cancer death worldwide in 2020, as well as the 1st and 3rd most common cancer in men and women, respectively. There were 2.2 million newly diagnosed cases and 1.7 million cancer deaths reported for lung cancer [1]. The National Lung Screening Trial (NLST) reported a reduction in lung cancer mortality with chest computed tomography (CT) screening in the participants with high cancer risk [2]. Since 2013, the Preventive Services Task Force (USPSTF) has recommended low-dose computed tomography for lung cancer screening [3]. With the increased application of chest CT for lung cancer screening, pure ground-glass nodules (pGGNs) were frequently found [4]. The cause of pGGN varied, including not only benign lesions such as focal interstitial fibrosis, infection, and inflammation, but also lung cancer and its precursors [5]. In 2011, the International Association for the Study of Lung Cancer (IASLC), American Thoracic Society (ATS), and European Respiratory Society (ERS) established a new categorization for adenocarcinoma of the lung, including preinvasive lesions with atypical adenomatous hyperplasia (AAH) and adenocarcinoma in situ (AIS), minimally invasive adenocarci- noma (MIA), and invasive adenocarcinoma (IA) [6]. AAH, AIS, MIA, and IA may feature pGGN [7,8]. With adequate surgical resection, the patients with AIS and MIA have 100% or near 100% disease-free survival [9–11], and those with localized IA were associated with a 5-year survival rate of 70–90% [12,13]. If left untreated, the median survival of early lung cancer is merely 13 months in patients with T1 disease [14]. Therefore, it is crucial to identify IA earlier for a better outcome. It is a technical challenge to perform a core needle biopsy for a pGGN < 2 cm [15,16]. Therefore, some investigators have tried to identify IAs or malignant nodules presenting as pGGNs. Some authors attempted to differentiate preinvasive adenocarcinomas from IAs that present as pGGNs [4,17–24], while others investigated the correlation between the pathological findings and nodules presenting as solid, part-solid and pGGNs [25,26]. Our study aimed to analyze the CT findings of pGGN < 2 cm and differentiate IA from non-IA (NIA) for the appropriate management of pGGNs. 2. Materials and Methods 2.1. Patient Selection This study was approved by the Institutional Review Board of Chang Gung Med- ical Foundation (IRB No: 202001934B0 issued on 9 November 2020) and in compliance with the Health Insurance Portability and Accountability Act. In a period of 69 months, from December 2013 to August 2019, patients who underwent preoperative CT-guided localization for lung nodule excision were retrospectively reviewed. The inclusion criteria were shown as follows: (1) pGGN with a mean diameter <20 mm. The mean diameter was defined as the average of the long axis and short axis diameters, measured on a lung window CT image. (2) Slice thickness of 0.625 mm on non-enhanced chest CT. (3) The presence of definite pathological diagnoses. According to the inclusion and exclusion Cancers 2021, 13, x FOR PEER REVIEW 3 of 12 Cancers 2021, 13, 3945 3 of 12 CT image. (2) Slice thickness of 0.625 mm on non-enhanced chest CT. (3) The presence of definite pathological diagnoses. According to the inclusion and exclusion criteria shown criteriain the flowchart shown in in the Figure flowchart 1, the in CT Figure images1, the with CT a imagesslice thickness with a slicegreater thickness than 0.625 greater mm thanand 0.625nodules mm with and solid nodules components with solid or components inconclusive or inconclusivepathological pathologicalresults were resultsall ex- werecluded. all excluded.Both benign Both and benign malignant andmalignant pGGNs were pGGNs included were in included this study. in this Finally, study. a Finally,total of a181 total nodules of 181 in nodules 171 patients in 171 patientswere enrolled were enrolledin this study. in this The study. clinical The clinicaldata of dataeach ofpatient each patientwere recorded; were recorded; these included these included age, gender, age, gender, smoking smoking history, history, drinking drinking history, history, cancer cancer his- history,tory, and and the the pathological pathological results results of ofthe the nodules.
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